Brucellosis is a zoonotic disease of considerable economic and public health significance globally. Despite the limited bacteriological evidence, a large number of serological works revealed that it is prevalent both in livestock and humans in Ethiopia. The current comprehensive review was carried out to provide apparent pooled seroprevalence (APS) estimates at individual animal and herd levels in livestock, and identify factors causing variability between studies conducted over the last two decades, show the spatial distribution, as well as summarizes Brucella species reported from livestock. It also provides APS of brucellosis in humans and evaluates the public health awareness of zoonotic brucellosis. In this review, systematic and synthetic review approaches were followed to summarize the available information. For the systematic review and meta‐analysis, articles were selected based on predefined criteria. Data extracted from these articles were analysed using meta‐analytical approaches to provide APS estimates and in‐between study variations for humans and all livestock species considered. Sensitivity analyses and bias assessments were conducted using influence plot analysis and, Egger's and Begg's statistics along with funnel plots, respectively. Synthetic review approaches were used to summarize data on isolates and public health awareness. Pooled seroprevalence estimate of brucellosis at national level was 2.6% (95% CI: 2.2–3.0) in cattle, 4% (95% CI: 3.1–5.1) in goats, 3% (95% CI: 2.3–3.9) in sheep and 3% (95% CI: 2.4–3.7) in camels. At a herd level, 16.3% (95% CI: 12.9–20.5) of cattle, 12.1% (7.1–19.9) of goat, 13.3% (7.6–22.1) of sheep and 19.7% (13.8–27.4) of camel herds in the country had at least one seropositive animal. Cattle in the pastoral/agropastoral production systems had significantly higher (p < .05) APS compared to mixed crop‐livestock and urban/peri‐urban dairy production systems. Pooled seroprevalence of brucellosis in small ruminants (8.3%, 95% CI: 6.3–10.8) and camels (4.4%, 95% CI: 3.5–5.6) in Afar were significantly higher (p < .05) than in other regions. Reports conducted using ELISA and serial Rose Bengal plate test (RBPT)‐ELISA had higher (p < .05) APS estimates than serial RBPT and complement fixation test. Brucella melitensis and B. abortus were reported from goats and cattle, respectively, from three available reports. The APS of brucellosis in humans was 5% (95% CI: 3.3–7.3). Public awareness of brucellosis was low (18.4%), while, practices that expose humans to Brucella infection were high. Scenario‐based control interventions on regions and production systems using one health approach are suggested.